The biological and behavioral basis of upper limb asymmetries

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Neuroscience and Biobehavioral Reviews 32 (2008) 598–610

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Review

The biological and behavioral basis of upper limb asymmetries insensorimotor performance

Daniel J. Goble�, Susan H. Brown

Division of Kinesiology, University of Michigan, 401 Washtenaw Avenue, Ann Arbor, MI 48109-2214, USA

Received 14 May 2007; received in revised form 26 September 2007; accepted 28 October 2007

Abstract

Asymmetries in upper limb performance are a fundamental aspect of human behavior. This phenomenon, commonly known as

handedness, has inspired a great deal of research over the course of the past century garnering interest across a multitude of scientific

domains. In the present paper, a thorough review of this literature is provided focusing on the current state of knowledge regarding

neuro-anatomical and behavior-based arm asymmetries. It is hoped that this information will provide a basis for new insights regarding

the design and implementation of future studies regarding arm laterality.

Published by Elsevier Ltd.

Keywords: Handedness; Motor control; Laterality; Anatomical structure; Sensorimotor function

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598

2. Right arm biases for movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599

2.1. The genetic basis of arm preference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599

2.2. Environmental influences on arm preference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599

3. An enhanced role for the left hemisphere in movement control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 600

4. Anatomical correlates of handedness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 600

5. Arm asymmetries in motor output . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 602

6. The dynamic-dominance hypothesis of handedness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 602

6.1. Preferred arm specialization for trajectory control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 602

6.2. Non-preferred arm specialization for positional control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 603

7. Open versus closed-loop model of handedness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 603

8. Upper limb asymmetries in the utilization of sensory feedback . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604

8.1. Arm asymmetries in visual feedback processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 605

8.2. Arm asymmetries in proprioceptive feedback processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 606

9. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 606

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 606

e front matter Published by Elsevier Ltd.

ubiorev.2007.10.006

ing author. Tel.: +1734 277 7432.

ess: [email protected] (D.J. Goble).

1. Introduction

The ability to perform skilled movements of the upperlimbs is a defining feature of modern day humans, and hasbeen since the time of their upright standing ancestors

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ARTICLE IN PRESSD.J. Goble, S.H. Brown / Neuroscience and Biobehavioral Reviews 32 (2008) 598–610 599

some 2.5 million years ago (Bradshaw and Rogers, 1996).Given the gross anatomical symmetry of the arms,however, it is perhaps surprising that the left and rightarms did not evolve to have similar degrees of dexterity.Rather, the two arms often demonstrate vast differences insensorimotor ability, a quality that has been defined as‘‘handedness’’ and one which has been the subject ofintense study within the realms of psychology, neurophy-siology and others. The focus of the present paper,therefore, is to review this vast scientific literature with aparticular emphasis on upper limb asymmetries in sensor-imotor behavior. For reasons that will become moreapparent in the section to follow, most research in thisarea has been biased towards the study of individuals withright-arm preference and, thus, it will generally be beyondthe scope of this review to discuss studies involving left-handed individuals. Briefly, however, it should be notedthat individuals with left-arm preference appear lesslateralized and more variable than their right-handedcounterparts, and are not the simple genetic (McManus,1995) or behavioral inverse (Perelle and Ehrman, 2005).

2. Right arm biases for movement

While limb asymmetries in motor behavior are evident tosome extent in many animal species (see Vallortigara andRogers, 2005 for a review), humans appear unique in that aclear population level bias exists for using one arm versusthe other. Indeed, based largely on self-report question-naires, it has been estimated that 9 out of 10 individuals areright-handed such that the right arm is preferred over theleft when performing tasks such as reaching for a target ormanipulating an object (Annett, 1985; Gilbert andWysocki, 1992; Oldfield, 1971). Remarkably, this propor-tion of right-handed individuals has remained stable acrossgeographical locations/cultures (Bryden et al., 1996; Hattaand Nakatsuka, 1976; Ida and Bryden, 1996; Marchantet al., 1995) and has persisted over the course of time. Withrespect to this latter point, Coren and Porac (1977) showeda greater number of right versus left-arm depictions ofmotor activity in various artworks spanning the past 5000years and archeological evidence has indicated thateven the first humans, on earth some 35,000 years ago,were likely right-handed with respect to stone tool use(Semenov, 1964; Toth, 1985).

2.1. The genetic basis of arm preference

Despite the enduring nature of right arm preference, noconsensus has been reached regarding its origin. Onecontroversial point of view that has been posited by severalresearchers suggests that right-handedness is a geneticallyfixed trait and, therefore, left-handedness represents apathological or diseased state (Bakan et al., 1973; Coren,1996). Interestingly, this hypothesis accounts for a numberof correlational findings indicating a relationship betweenbirth trauma and a higher incidence of left-handedness

(Colburne et al., 1993; Coren, 1996; Dellatolas et al., 1993).In addition, there has long been thought to be anassociation between left-arm preference and cognitivedisorders such as schizophrenia (Green et al., 1989; Orret al., 1999) and autism (Fein et al., 1984; Soper et al., 1986;Waterhouse and Fein, 1984).In contrast to various fixed trait approaches to handed-

ness, theories grounded in Mendelian genetics haverepresented a more promising means of explaining rightarm preferences with the ‘‘right shift theory’’ of Annett(1972) being, perhaps, the foremost. This model postulatesthat one allele (RS+) leads to the development of botharm praxis and language abilities in the left cerebralhemisphere (i.e. controlling the right arm), and a secondallele (RS-) allows for arm and language abilities to berandomly distributed in either hemisphere (Annett, 1978,1998). Unfortunately, however, this and other relatedgenetic models (e.g., McManus, 1995) are often criticizedfor two seemingly fatal flaws. First, there has been nosuccess to date in isolating the supposed gene or genesresponsible for implementing a right arm tendency.Second, in a meta-analysis of studies on monozygotic(identical) twins, Coren and Halpern (1991) found thatonly 75% of the paired offspring expressed the same armpreference despite a 100% overlap in genetic make up.Until these issues can be adequately resolved, the case for agenetic basis of handedness will no doubt remain highlydebated.

2.2. Environmental influences on arm preference

In lieu of a purely genetic explanation for right armasymmetries in motor behavior, the influence of environ-mental and socio-cultural factors on handedness has alsobeen explored. One observation that has inspired a greatdeal of research in this area is the finding that a higherpercentage of right-handed individuals exists for olderpeople at the end of the age spectrum (Beukelaar andKroonenberg, 1986; Dellatolas et al., 1991; Ellis et al.,1988; Gilbert and Wysocki, 1992). Based on this finding, ithas been argued that many natural left-handers have beenforced to adopt right-arm preference over the course of alifetime in order to accommodate for living in a right-handed world, and/or to avoid the religious and socialstigmas associated with left-handedness or ‘‘sinistrality’’(Coren, 1993; Harris, 1990). While these proposed socio-cultural influences have garnered support from reportsindicating that left-handed individuals are more prone toaccidental death, and subsequently live, on average, 7 yearsfewer than their right-handed counterparts (Coren andHalpern, 1991; Halpern and Coren, 1988), a socio-culturalaccount for right arm preference remains, by itself,unconvincing. Particularly concerning is the finding thateven when environmental pressures are relatively harsh,and are present at an early age, arm preference is not easilychanged (Porac et al., 1986). Indeed, Porac et al. (1990)reported that most attempts to change handedness fail, or

ARTICLE IN PRESSD.J. Goble, S.H. Brown / Neuroscience and Biobehavioral Reviews 32 (2008) 598–610600

result in motor skill performance that lags behind that ofthe originally preferred arm. Overall, therefore, it seemsmost likely that both nature (genetics) and nurture(environment) play substantial and, likely, complementaryroles in the expression of arm preference and performanceasymmetries.

3. An enhanced role for the left hemisphere in movement

control

In light of the discovery by Broca (1861), and laterWernicke (1874), that the left hemisphere is specialized forvarious aspects of language, Liepmann (1908) was the firstto suggest that asymmetries in motor behavior might alsobe sub-served by hemispheric processing differences.Specifically, it was hypothesized that the hemispherecontralateral to the preferred arm (most often the left)played an enhanced role for both preferred and non-preferred arm movements. Liepmann (1920) later justifiedthis view on the basis of observations made with respect toindividuals having unilateral brain injury due to stroke. Inthis work, individuals with left, but not right, hemisphericdamage were found to be unable to correctly perform thespatiotemporal aspects of skilled movement with eitherarm, a condition termed ‘‘ideomotor apraxia’’. Further,injury to the left hemisphere resulted in an inability tomake precise, independent movements of both hands (i.e.‘‘limb kinetic apraxia’’), whereas only the contralateral lefthand was affected when the injury was to the righthemisphere. While these findings have garnered supporton a number of subsequent occasions (Haaland et al., 1977;Haaland and Delaney, 1981; Hanna-Pladdy et al., 2002;Wyke, 1971), it should be noted that more recent reportssuggest that both hemispheres make significant contribu-tions to the control of goal-directed movement (Fisk andGoodale, 1988; Haaland and Harrington, 1989a, b, 1994,1996; Haaland et al., 2004; Winstein and Pohl, 1995). Theresults of these studies will be addressed in greater detail ina later section (see Section 7).

With the advent of various non-invasive brain mappingand cortical stimulation techniques it is now possible toexplore hemispheric differences in those individuals withnormal brain function in vivo. Using functional magneticresonance imaging (fMRI), for example, Kim and collea-gues (1993) measured activation of the left and right motorcortices in response to finger/thumb opposition movementsmade by each hand. For this study it was found that,similar to previously described results for stroke patients,the left hemisphere of right-handers played an enhancedrole in movement control. Specifically, right motor cortexwas primarily active for movements of only the contral-ateral left hand, whereas left motor cortex activation wasseen for movements of either hand. Transcranial magneticstimulation (TMS) studies have also reported left hemi-sphere dominance for increasing the magnitude of motorevoked potentials (MEPs) in ipsilateral hand musclesduring the performance of a motor task with the opposite

hand. In particular, it has been shown for right-handedindividuals that single pulse TMS to the left compared toright motor cortex more often induces facilitation of MEPsin hand muscles (e.g. opponens pollicis, first dorsalinterosseous) in both the left and right arms. In contrast,right hemisphere stimulation elicits a response in only thecontralateral left arm (Ghacibeh et al., 2007; Ziemann andHallett, 2001).The particular function of left motor cortex activation

during left arm movement in right-handed individualsremains uncertain. Contrary to the findings of Dassonvilleet al. (1997), who showed a correlation between ipsilateralactivation and the strength of arm dominance, direct lefthemispheric control of the left arm seems unlikely based onreports that only 10–15% of corticospinal projectionsremain uncrossed at the level of the medulla (Nyberg-Hansen and Rinvik, 1963). Alternatively, it has beenhypothesized that the left hemisphere might have someinfluence over the right hemisphere via the corpuscallosum. In this case, it is thought that both hemispheresare active prior to movement initiation, at which point onehemisphere is inhibited by the other in order to execute aunilateral movement of the contralateral arm (Britton etal., 1991; Rossini et al., 1988). Based on this line ofreasoning, it would seem that involvement of the lefthemisphere during ipsilateral arm movements reflects arelative inability of the right hemisphere to inhibit the left(Chen et al., 1997). This notion is supported by severalpaired pulse TMS studies where sequential stimulation ofthe hemispheres has shown greater inhibition of the motorcortex in the right versus left hemisphere (Kobayashi et al.,2003; Netz et al., 1995).

4. Anatomical correlates of handedness

Given the asymmetries in hemispheric function describedabove, exploration into a potential anatomical substratefor handedness has been undertaken at both macroscopicand microscopic levels. One gross structural componentthat initially received particular attention is the planumtemporale (PT), which is located on the posterior portionof the temporal lobe. Based on postmortem studies, a moreabrupt and anterior upward curving of the PT has beenreported for the right hemisphere, in contrast to a longerand larger left PT (Falzi et al., 1982; Geschwind andLevitsky, 1968; Wada et al., 1975). Given that the PTcoincides largely with the speech region of Wernicke(1874), it has been speculated that this asymmetry reflectsleft hemispheric specialization for language (Galaburdaet al., 1978; Geschwind and Galaburda, 1985). This ideacomplements well several recent theories that have beenproposed regarding the evolution of language from themanual gesture system in non-human primates found inarea F5, which corresponds with Broca’s area in humans(Gentilucci and Corballis, 2006; Rizzolatti and Arbib,1998). With respect to handedness, however, Steinmetz andcolleagues (1991) and Steinmetz (1996), were not able to


show a positive correlation between left PT volume and thedegree (i.e. strength) of right-handedness as measured byboth a speeded finger tapping and a pen and paper handdominance test.

Impressions on the inner surface of the skull called‘‘petalia’’ provide a negative of the brain’s surface topologyrevealing regional asymmetries in hemispheric shape andsize. Although petalia in the right frontal and left occipitallobes are seen in nearly all individuals, they are mostprominent in right-handers (Kertesz et al., 1986; Lemayand Kido, 1978). This observation further corroboratesevidence of a positive correlation between the distributionof the lobes and right-handedness. Specifically, in indivi-duals with right arm preference, the occipital lobe isconsiderably wider in the left hemisphere, whereas thefrontal lobe is wider in the right hemisphere (Galaburda etal., 1978). In addition, the left hemisphere has been foundto protrude more often in the posterior direction, while ananterior protrusion is common for the right hemisphere(LeMay, 1976). This anatomical configuration, known as‘‘Yakovlevian torque’’, is demonstrated in Fig. 1 and givesthe illusion that the brain is rotating in a counter-clockwisedirection.

The motor cortex is perhaps the most well-studied areaof the brain with respect to hemispheric differences, dueprimarily to its many projections leading to the spinal-motor neurons. In a postmortem study measuring theextent of cortical surface within the dorsolateral portionof the central sulcus, an anatomical marker of primary

Fig. 1. Transverse anatomical MRI image of a typical brain demonstrat-

ing Yakovlevian torque. Note the greater posterior displacement of the left

(L) hemisphere and greater anterior displacement of the right (R)

hemisphere giving rise to the appearance of a counter-clockwise rotation

of the brain indicated by dotted arrows.

sensorimotor cortex size, a larger surface area was foundfor the left versus right hemisphere (White et al., 1994).However, a subsequent report by this group with a greaternumber of subjects found no asymmetry in the dorsolateralcentral sulcal surface area between the two hemispheres(White et al., 1997). Not withstanding these results,magnetic resonance morphometry has been used tomeasure precentral sulcal depth in the right and lefthemisphere in vivo (Amunts et al., 2000; Amunts et al.,1996). This analysis revealed that in individuals with rightarm dominance the precentral sulcus of the left hemisphereappears deeper compared to the right, and that thisrelatively macroscopic asymmetry is accompanied by amicroscopic difference in neurophil volume (Amunts et al.,1996). The latter finding was interpreted as reflecting agreater percentage of fibrous processes, and more profusehorizontal connections, in the left hemisphere providing apotential substrate for the representation of more complex,preferred arm movements (Hammond, 2002).The threshold for eliciting a motor response in various

intrinsic and extrinsic muscles of the preferred and non-preferred arms via TMS of the motor cortex has also beenstudied. In general, this work has shown that preferred armmusculature is activated at a lower threshold of contral-ateral brain stimulation (Cantello et al., 1991; Macdonell etal., 1991; Triggs et al., 1994), although other studies havefailed to reveal arm differences (Cicinelli et al., 1997;Civardi et al., 2000). In addition, TMS has been used as ameans of mapping the extent of various hand and armrepresentations in the motor cortex. One particularlyinfluential study in this area was conducted by Triggset al. (1999) who quantified the number of cortical siteseliciting a motor response in the abductor pollicis brevisand flexor carpi radialis muscles of the left and right arms.In this case, right-handed subjects had a larger cortical areain the left hemisphere devoted to the targeted muscles thanthat seen in the right hemisphere, a finding that isconsistent with comparable studies using magneto-ence-phalography (Volkmann et al., 1998) and fMRI (Dasson-ville et al., 1997; Krings et al., 1997) techniques.In association with these motor cortical asymmetries, left

versus right side differences have been shown in the patternof corticospinal fiber tract decussation. In an early studyinvolving human neonates, for example, Flechsig (1876)noted a distinct asymmetry in the distribution of corti-cospinal projections at birth with the left medullarypyramid being larger, and showing greater decussation,than the right. Nearly a century later, this same asymmetricpattern of fiber decussation was also shown for more than70% of adult specimens tested postmortem (Kertesz andGeschwind, 1971), a finding that was recently corroboratedby Nathan et al. (1990). Given that the crossed fibers fromboth pyramids largely innervate motor units correspondingto the hand in the spinal cord (Brinkman et al., 1970),an additional aim of these studies was to correlate thedegree of decussation to subject handedness. However,due possibly to the small number of left-handed subjects


available for study, no significant association between armpreference and corticospinal organization was found.

Preferred versus non-preferred arm differences in thespinal-motor circuitry may also contribute to arm perfor-mance asymmetries given evidence suggesting greaterpreferred arm excitability of the motor-neuronal pool. Ina study assessing motor unit firing patterns of the firstdorsal interosseous muscle, Adam and colleagues (1998)found evidence of a preferred arm advantage for motorunit recruitment threshold, initial firing rate, average firingrate at target force and discharge variability. Indeed, theseresults are in agreement with those showing greaterHoffmann reflex responses for the preferred versus non-preferred arm (Tan, 1989a, b), although no arm differencein h-reflex response between arms has also been reported(Aimonetti et al., 1999). Further, evidence suggests that thesynchronization of motor units within the extensor musclesof the preferred arm is greater during isometric contrac-tions (Schmied et al., 1994) and that the tendon tap reflexresponses of the preferred versus non-preferred arm aregreater in magnitude (Aimonetti et al., 1999). To whatextent these asymmetries reflect shifts in muscle fibercomposition due to repetitive, low-intensity use of pre-ferred versus non-preferred arm is not yet clear. However,at least one study has demonstrated an increased percen-tage of slow twitch fibers in the extensor carpi radialisbrevis muscle of the preferred wrist, a key muscle duringthe production of grip postures (Fugl-Meyer et al., 1982).

5. Arm asymmetries in motor output

In line with the functional/anatomical differences out-lined above, one of the most traditional approaches to thestudy of handedness has been the quantification of armdifferences in the generation of motor output. A well-known demonstration of this lies in the now classic studiesof Woodworth (1899) who assessed the ability of subjectsto accurately draw lines of equivalent length with either thepreferred or non-preferred hand. In this case, it was foundthat movements of the preferred right hand were substan-tially more accurate than those of the non-preferred left,and that this asymmetry was enhanced in conditions wheresubjects were forced to move at faster velocities. Combinedwith the observation that the absence of visual feedbackdid not alter the observed asymmetry, Woodworth (1899,p. 34) was led to conclude ‘‘the seat of superiority of theright hand is probably in the motor centers’’.

Subsequent to Woodworth (1899), motor behavioralresearch has revealed numerous right arm advantages inthe generation of motor output including increases in thestrength, speed and consistency of movement. Whencomparing maximum grip forces in healthy subjects, forexample, it has been well accepted that the preferred armcan produce forces that are approximately 10% larger thanthose of the non-preferred arm (Armstrong and Oldham,1999; Crosby et al., 1994; Incel et al., 2002; Petersen et al.,1989). In addition, with respect to the magnitude and

timing muscle force production, numerous finger tappingexperiments have demonstrated preferred arm advantagesin the speed and consistency of performing repetitive fingerflexion and extension movements (Peters, 1976; Peters andDurding, 1979; Provins, 1956; Todor and Kyprie, 1980;Todor et al., 1982). Indeed, a link between these behavioralfindings and the force generating characteristics of thepreferred versus non-preferred arm was made by Toderand Smiley-Oyen (1987), who directly measured the fingerforces associated with tapping. In this case, a positiverelationship between preferred arm tapping ability and thegeneration of mean force levels with decreased variabilitywas found.Beyond studies of finger tapping, arm asymmetries in

motor output have also been revealed though varioustargeted reaching experiments. In an influential study byAnnett et al. (1979), the amount of time necessary to placepegs in relatively small holes was found to be significantlyshorter for the preferred right arm of right-handedindividuals. Further, the increased movement time for thenon-preferred arm did not appear to be due to subjectsmaking longer duration corrective movements but, rather,having to make more of them. In this case, it was arguedthat non-preferred arm motor output was subject toincreased variability and, thus, necessitated a greaternumber of corrective movements. This interpretation hasbeen utilized on at least two subsequent occasions forresults indicating a preferred arm advantage in the speed ofreaching and pointing to a visual target (Carson et al.,1993a; Roy and Elliott, 1989).

6. The dynamic-dominance hypothesis of handedness

Sainburg (2002) first proposed the dynamic-dominancehypothesis of handedness based on several fundamentaldifferences in movement strategy that were observedbetween the preferred and non-preferred arms of right-handed individuals. Unlike many other behavioral ap-proaches to handedness research, where performance of thenon-preferred arm is thought to be inferior for mostaspects of movement, this hypothesis proposes that eacharm is specialized for a different aspect of movementcontrol. Indeed, given that most activities of daily livingrequire the use of both hands, such a dichotomy of armfunction would seem to be more advantageous than relyingon a single dominant arm. With respect to arm preferenceand bilateral tasks, the non-preferred left arm has beenshown to provide both a frame of reference for interactionswith the preferred arm, as well as show ‘‘precedence’’, suchthat its actions precede those of the preferred arm (Guiardand Ferrand, 1996; Guiard, 1987).

6.1. Preferred arm specialization for trajectory control

Evidence of preferred arm specialization for the controlof movement trajectory was initially revealed in a studycomparing the coordination patterns employed by the


preferred and non-preferred arms during targeted reaching(Sainburg and Kalakanis, 2000). In this work, it wasdemonstrated that movements made by the preferred rightarm in right-handed subjects showed a distinctly differentpattern of joint torques than those produced by the non-preferred arm. Specifically, when reaches were made totargets where the amount of elbow displacement was heldconstant (201), but where the amount of shoulder excursionwas systematically varied (51, 101 and 151), significantlydifferent coordination patterns emerged. For preferred armreaching, straight-line hand path trajectories were achievedthrough a more efficient inter-limb torque pattern asmovements of both the proximal and distal arm segmentswere controlled with forces generated primarily at theshoulder. In contrast, the hand paths produced by the non-preferred arm had greater overall curvatures, which wereassociated with increased shoulder excursion due to amovement strategy that did not make efficient use of inter-segmental interaction forces.

The findings of Sainburg and Kalakanis (2000) werelater expanded by Sainburg (2002) in the initial formaliza-tion of the dynamic-dominance hypothesis of handedness.In this study, subjects performed reaching to eight targetsin a virtual environment that allowed for visual feedbackregarding only target position and endpoint location of theindex finger. This procedure was completed under twoexperimental conditions that attempted to determine theinfluence of visuomotor transformations versus novel inter-segmental dynamics on arm performance. To assessvisuomotor transformations, a visuomotor rotation taskwas utilized where subjects were required to adapt to afeedback display of finger position rotated 301 relative tothe start position. On the other hand, novel inter-segmentaldynamics were assessed using a mass adaptation paradigmwhere subjects had to adapt to an unseen 1 kg massattached to the arm. In comparing these two tasks, cleardifferences were seen between visuomotor and massadaptation, such that arm performance asymmetries wereevident only during mass adaptation. This asymmetrymirrored that demonstrated by Sainburg and Kalakanis(2000) in that the preferred arm used significantly lessmuscle torque than the non-preferred arm. It was, there-fore, concluded that ‘‘manual asymmetries arise, down-stream in the motor control sequence to visuomotortransformations, when the trajectory plan is transformedinto dynamic properties’’ (Sainburg, 2002, p. 253).

The extent of right arm dominance for trajectory controlhas been the focus of subsequent studies by Sainburg andcolleagues (Bagesteiro and Sainburg, 2002; Sainburg andWang, 2002; Wang and Sainburg, 2003). For example, in areaching task that varied with respect to the amount ofinter-segmental torque necessary to obtain a target posi-tion, Bagesteiro and Sainburg (2002) showed more efficienttorque strategies were utilized by the preferred arm/hemisphere system independent of arm kinematics. Inaddition, a series of studies (Sainburg and Wang, 2002;Wang and Sainburg, 2003, 2004) have shown an asym-

metric transfer of learning for visuomotor rotations. Inthese studies opposite arm training of a rotated visualdisplay resulted in an enhanced ability of the preferred armto specify the initial direction of the targeted movementtrajectory. Taken together, these results provide strongsupport for a preferred arm advantage in the specificationand control of arm trajectory.

6.2. Non-preferred arm specialization for positional control

In light of the advantages ascribed to the preferred armin the control of limb trajectory dynamics, a role for thenon-preferred arm in the control of static posture has alsobeen suggested. Support for this hypothesis was firstprovided by Bagesteiro and Sainburg (2003) in anassessment of inter-limb differences in load compensation.In this study, a virtual cursor representing endpointlocation of the finger was moved to a target position of201 elbow flexion. On random trials a 2 kg mass wasattached to the subject’s forearm such that the subject hadno knowledge of the added load. When faced with thismass perturbation only the non-preferred arm was able toachieve a level of endpoint accuracy similar to that foundin the non-loaded condition, while the preferred armshowed consistent overshooting of the target. Based onelectromyographic and kinematic analyses, the non-pre-ferred arm was found to compensate for the unknown loadthrough changes in muscle activation occurring post-peaktangential velocity. These observations were interpreted asreflecting a specialized role for the non-preferred arm insensory feedback-mediated error correction.Additional support for a non-preferred arm advantage in

the control of static position comes from studies regardingthe inter-limb transfer of movement strategy (Sainburg andWang, 2002; Wang and Sainburg, 2003). In these studies,arm asymmetries were assessed in the transfer of move-ment-related information following adaptation to a visuo-motor rotation. In this case, following training with theopposite arm, enhancement in endpoint accuracy com-pared to naı̈ve performance was reported, but only for thenon-preferred arm. While this finding was not supported ina study involving visuomotor adaptation to single versusmultiple targets (Wang and Sainburg, 2004), subsequentstudies have found similar non-preferred arm advantagesin the transfer of limb position information including tasksinvolving inertial dynamics and load compensation (Ba-gesteiro and Sainburg, 2005).

7. Open versus closed-loop model of handedness

In contrast to studies of individuals with unilateral braininjury indicating greater arm deficits for left versus righthemisphere damage (Haaland et al., 1977; Haaland andDelaney, 1981; Liepmann, 1908, 1920; Wyke, 1971), morerecent behavioral studies by Haaland and Harrington(1989a, b, 1994) and Winstein and Pohl (1995) havesupported the notion that each hemisphere may be


specialized for different aspects of motor control. In thesestudies, comparisons were made between the visuallyguided reaching movements of healthy individuals andthose of individuals with right or left hemispheric damagedue to stroke. Overall, left hemisphere damage resulted indeficits in the early stages of movement most commonlyassociated with open-loop (i.e. relatively feedback inde-pendent) control. These deficits included increased reactiontimes (Haaland and Harrington, 1989a, 1994) and a slowerinitial movement component (Winstein and Pohl, 1995). Incontrast, individuals with damage to the right hemisphereshowed poorer closed-loop (i.e. feedback dependent)control, as would be necessary for accurately achieving afinal target position (Haaland and Harrington, 1989b;Winstein and Pohl, 1995).

Unfortunately, as is the case with most clinically derivedmodels of motor function, the open versus closed-loophypothesis model remains limited due to rather incon-sistent findings. This likely reflects the inherent variabilityassociated with studies of brain-injured individuals wherenaturally occurring lesions are relatively diffuse in nature.Indeed, in the previously described studies by Haaland andHarrington (1989a, b, 1994) and Winstein and Pohl (1995),lesions were located throughout the cortex and in a numberof sub-cortical regions including the basal ganglia and thecerebellum. Further, in a review article on the hemisphericcontrol of movement in individuals with brain injury,Haaland and Harrington (1996) noted several examples ofconflicts in the literature including a contradictory study byFisk and Goodale (1988). In this study, the findingsreported were in direct opposition to those forming thefoundation of the open versus closed-loop hypothesis,despite using paradigm similar to that of Haaland andHarrington (1989a, b, 1994) and Winstein and Pohl (1995).Specifically, this study found that the ability to perform theopen-loop component of a movement was affected by rightrather than left hemisphere damage, while left hemisphereinjury led to difficulties in the closed-loop control of themovement. Interestingly, the results of Fisk and Goodale(1988) are more in line with several studies of visuallyguided reaching in healthy right-handed subjects whereshorter reaction times for the non-preferred left arm havebeen reported. In this case, it has been suggested that aright hemisphere advantage exists for the allocation ofattentional resources or specification of the spatial aspectsof the movement to be performed. (Barthelemy andBoulinguez, 2001, 2002; Boulinguez and Nougier, 1999;Bradshaw et al., 1990; Goble, 2007; Carson et al., 1990,1993b, 1995; Velay et al., 1999, 2001; Mieschke et al.,2001).

8. Upper limb asymmetries in the utilization of sensory

feedback

There has been increasing interest over the past severaldecades in the role that sensory feedback might play indetermining arm performance asymmetries. Perhaps the

most influential study in this area was conducted byFlowers (1975) who assessed arm performance during a‘‘ballistic’’ (i.e. relatively feedback independent) tappingtask, and a more ‘‘corrective’’ (i.e. relatively feedbackdependent) visual aiming task. In the tapping task, subjectswere asked to tap the preferred or non-preferred finger asfast as possible without aiming the movement to hit aparticular point. In this case, little control of the positionor force of each tap was required. In contrast, during thevisual aiming task, a Fitts paradigm (Fitts, 1954) was usedwhere subjects made fast and accurate reaching movementsbetween two targets that varied in width and movementamplitude. Overall, it was found that the preferred armperformed significantly greater than the non-preferred armbut, only in the aiming task. This led Flowers (1975, p. 39)to conclude ‘‘that the essential dexterity difference betweenthe preferred and non-preferred hands is in the sensory orfeedback control of movement’’.Following on the work of Flowers (1975), feedback-

based advantages for the preferred arm/hemisphere systemhave been suggested on several other occasions basedprimarily on the observation that arm differences inreaching accuracy are most apparent during the latterstages of movement when sensory feedback is thought to beof particular importance. While an early description of thisphenomenon was provided by Woodworth (1899) andTodor and Cisneros (1985) were the first to quantify armdifferences during the corrective phase of movement byhaving right-handed subjects perform fast and accuratereaching using an accelerometer-mounted stylus. Based onthe results of this study, it was shown that the longermovement durations seen for the non-preferred arm whenobtaining relatively small visual targets were associatedwith greater time spent ‘‘homing in’’ the target during thedeceleratory phase of movement. Taken together withensuing studies reporting a similar preferred arm advan-tage in the amount of time spent the post-peak velocityphase of movement (Boulinguez et al., 2001; Elliott et al.,1995; Mieschke et al., 2001; Roy et al., 1994), it seemsreasonable to conclude that the preferred arm is moreefficient in using online feedback to correct movementtrajectory. However, some caution should also be exercisedwhen inferring processes from movement kinematics, giventhe inherent relationship between sensory and motorcomponents.While the above, generalized feedback account of arm

performance asymmetry represents a significant shift inthinking from classical, motor-based explanations ofhandedness, it is limited by its inability to address howspecific modalities of sensory feedback might influencemovement. In general, vision and proprioception arethought to be the most important sources of sensoryfeedback during the performance of voluntary movement.Vision, for example, provides an external frame ofreference for movement including information regardingobjects size, orientation and three dimensional position(Goodale et al., 2004; Jeannerod et al., 1998). Alternatively,

ARTICLE IN PRESS

Fig. 2. Schematic depicting a greater relative reliance of the preferred right arm/left hemisphere on visual feedback for movement, while the non-preferred

left arm/right hemisphere is more adept at using proprioceptive information.

D.J. Goble, S.H. Brown / Neuroscience and Biobehavioral Reviews 32 (2008) 598–610 605

proprioceptive information from skin, muscle and jointreceptors plays an important role in the control ofinteraction torques (Sainburg et al., 1993, 1995), limbsegment timing (Cordo et al., 1994, 1995) and theacquisition of internal models of skilled movement(Kawato, 1999; Kawato and Wolpert, 1998). A schematicrepresenting how vision and proprioception appear to belateralized to the preferred versus non-preferred arm,respectively, is provided in Fig. 2 and will be the focus ofthe following sections.

8.1. Arm asymmetries in visual feedback processing

In a study by Honda (1982), an initial indication thatvisual information might have a differential influence onmovements of the preferred versus non-preferred arm wasprovided. In this study, eye and arm displacements wererecorded during a bilateral reaching task where coupledarm movements were made to symmetrical visual targets.Based on this paradigm, it was found that subjects spend agreater amount of time visually monitoring the preferredarm, and that this behavior was associated with increasedpreferred arm performance in terms of the time required toinitiate and complete the targeted movement. Further, in acondition where subjects were required to monitor themovements of only one arm versus the other, it was shownthat preferred arm movement times were more affected bya lack of visual feedback. Taken together, these resultssupport the notion that the preferred arm is more reliant onthe use of visual information during the production oftargeted movements.

In light of the findings of Honda (1982, 1984), severalexperiments have been conducted in which the amount ofvisual information available to subjects was altered duringtargeted reaching. In the first of two studies, Roy andElliott (1986) asked subjects to reach to visual targets withthe preferred or non-preferred arm under ‘‘full vision’’ or

‘‘no vision’’ conditions. In the full vision condition, thelights in the testing room were on throughout the reachingtask, whereas in the no vision condition the lights wereturned off at the time of movement initiation. Although theno vision condition had a profound effect on the subjects’overall movement accuracy, the results of this studyshowed a similar right arm advantage regardless of visualfeedback availability. In contrast to this result, however,Roy and Elliott (1989) showed enhanced right armaccuracy in a third light availability condition where thelights were turned off 10 s prior to movement. Thissubsequent finding is in agreement with the findings ofHonda (1982, 1984) and suggests that the preferred arm ismore reliant on visual feedback during reaching.Perhaps a more intuitive means of determining arm

asymmetries in the utilization of movement-related visualfeedback is the manipulation of visual target size. In thiscase, when targets are relatively small, and movementspeed is emphasized, it has been reported on numerousoccasions that movements of the preferred arm relative tothe non-preferred arm are both faster and more accurate(Carson et al., 1993b; Elliott et al., 1995; Flowers, 1975;Mieschke et al., 2001; Roy et al., 1994; Todor andCisneros, 1985; Todor and Doane, 1978; Woodworth,1899). One clear example of this was provided in a study byTodor and Doane (1978) using a Fitts tapping paradigm.In this study, both the target width and movementamplitude were altered in such a way as to preserve taskdifficulty (i.e. the index of difficulty was held constant)while allowing the manipulation of visual feedbackconstraints (i.e. target size). Indeed, the results of thisstudy showed that arm asymmetries were related to thevisual demands of the task, as an increasing preferred armadvantages were seen with decreasing target size, but notwith increases in target amplitude. It was, therefore,concluded that visual feedback is of greater importanceto the control of preferred arm reaching movements.


8.2. Arm asymmetries in proprioceptive feedback processing

Proprioceptive feedback from muscle spindles (Burgesset al., 1982; Goodwin et al., 1972a, b; McCloskey, 1978),joint receptors (Skoglund, 1956), Golgi tendon organs(Houk and Henneman, 1967; Jami, 1992), and cutaneousmechanoreceptors (Edin and Abbs, 1991; Lynn, 1975) hasbeen shown to provide detailed information about theposition and velocity of body segments (Matthews, 1982,1988; Matthews and Stein, 1969; McCloskey et al., 1974),as well as the amount of tension within a muscle (Jami,1992). Despite these observations, however, the role ofproprioceptive information in determining arm perfor-mance asymmetries has been largely underappreciated, asmost studies of proprioceptive ability have focused solelyon the preferred right arm of right-handed individuals(Adamovich et al., 1998, 1999; Baud-Bovy and Viviani,1998; Darling, 1991; Lonn et al., 2000, 2001; Paillard andBrouchon, 1968, 1974; Rothwell et al., 1982).

Whereas studies assessing the role of visual information ontargeted movement have largely elicited asymmetries in favorof the preferred arm, the preponderance of evidence to datesuggests a non-preferred arm advantage in the ability toutilize feedback that is proprioceptive in nature. The firstevidence in support of this notion was provided by Roy andMacKenzie (1978) who examined arm differences in theability to match thumb and multi-joint arm positions in theabsence of vision. While in this study no asymmetries inmulti-joint arm position matching were found, a non-preferred left thumb accuracy advantage was seen. Basedon these preliminary results, Colley (1984) and Riolo-Quinn(1991) also reported greater accuracy for proprioceptivelyguided matches made by non-preferred thumb and Kurian etal. (1989) demonstrated non-preferred left arm dominancefor accurately reproducing elbow angles. Although Chap-man et al. (2001), and Carson et al. (1990), did not show armdifferences in an assessment of multi-joint position matchesmade in two and three dimensional space, recent studies bythis lab (Goble and Brown, 2007; Goble et al., 2006, 2005),have shown differences in elbow position matching abilityduring a task requiring interhemispheric transfer andmemory for proprioceptive target positions.

In the Goble and Brown (2007) study the extent to whichtask difficulty might explain the somewhat equivocalresults outlined above was explored by utilizing a varietyof matching tasks that varied with respect to propriocep-tive processing demands. In the first task, ipsilateralremembered matching, a similar method to that whichhas been previously employed was used where subjectsperformed memory-based matching of previously experi-enced elbow positions with the same arm. In contrast, thecontralateral concurrent matching task eliminated the needfor memory, as the target arm remained in the targetposition while subjects performed matching with theopposite arm. In this case, some degree of interhemispherictransfer was necessary in order to accurately achieve thetarget position. Lastly, in the contralateral remembered

condition, the demands of the first two tasks werecombined as subjects were asked to perform memory-based matching of a previously experienced arm positionwith the contralateral arm. Interestingly, it was in this mostdifficult condition requiring both memory and interhemi-spheric transfer of proprioceptive target information wherethe greatest non-preferred arm advantage was found. Thisresult emphasized the need to maximize proprioceptivefeedback processing demands when attempting to elicitarm asymmetries.Further support for a non-preferred arm advantage in

the utilization of proprioceptive feedback comes fromrecent neuro-imaging studies where greater right hemi-sphere (i.e. non-preferred left arm) activation has beenshown in association with tasks requiring enhancedproprioceptive feedback processing. For example, in astudy of right-handed volunteers, Butler et al. (2004) usedpositron emission tomography to assess the neuralcorrelates related to memory-based reaches made to targetsthat were either visual or proprioceptive in nature. Despitethe fact that all matching movements in this study weremade with the preferred right arm, it was found thatproprioceptively guided movements had increased activa-tion in the temporo-parietal area of the ipsilateral righthemisphere. Similarly, Naito et al. (2005) recently exploredhemispheric differences in the perceptive of movementillusions. In this study, greater right hemisphere activationwas found in a task where vibration of the hand extensormuscles was used to produce an illusion of wrist flexion (forreview of this technique see Goodwin et al., 1972a).

9. Summary

The goal of this paper was to review relevant literatureregarding the biological and behavioral basis of upper limbsensorimotor behavior. It was shown that, for the majorityof individuals, the right arm is preferred over the left whenperforming many activities of daily living, and that thisarm bias likely reflects structural/anatomical differences inthe neuromotor system. Despite the preponderance ofliterature that has focused on right arm motor dominance,however, one novel aspect of more recent studies onhandedness is the suggestion that the preferred and non-preferred arms have complementary roles during motorperformance. This can be seen in the dynamic dominanceand open versus closed-loop hypotheses of handedness, aswell as in studies assessing arm differences in visual versusproprioceptive feedback. Indeed, this more dualisticapproach to the study of upper limb performanceasymmetries represents a fundamental shift in thinkingregarding the study of handedness, which will no doubtinfluence future studies conducted in this area.

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